There are three basic strategies for biological pest control: classical (importation), where a natural enemy of a pest is introduced in the hope of achieving control; inductive (augmentation), in which a large population of natural enemies are administered for quick pest control; and inoculative (conservation), in which measures are taken to maintain natural enemies through regular reestablishment.[2]

Natural enemies of insect pests, also known as biological control agents, include predators, parasitoids, pathogens, and competitors. Biological control agents of plant diseases are most often referred to as antagonists. Biological control agents of weeds include seed predators, herbivores and plant pathogens.

Biological control can have side-effects on biodiversity through attacks on non-target species by any of the same mechanisms, especially when a species is introduced without thorough understanding of the possible consequences.

History[]

The term "biological control" was first used by Harry Scott Smith at the 1919 meeting of the Pacific Slope Branch of the American Association of Economic Entomologists, in Riverside, California.[3] It was brought into more widespread use by the entomologist Paul H. DeBach (1914–1993) who worked on citrus crop pests throughout his life.[4][5] However, the practice has previously been used for centuries. The first report of the use of an insect species to control an insect pest comes from "Nanfang Caomu Zhuang" (南方草木狀 Plants of the Southern Regions) (ca. 304 AD), attributed to Western Jin dynasty botanist Ji Han (嵇含, 263–307), in which it is mentioned that "Jiaozhi people sell ants and their nests attached to twigs looking like thin cotton envelopes, the reddish-yellow ant being larger than normal. Without such ants, southern citrus fruits will be severely insect-damaged".[6] The ants used are known as huang gan (huang = yellow, gan = citrus) ants (Oecophylla smaragdina). The practice was later reported by Ling Biao Lu Yi (late Tang Dynasty or Early Five Dynasties), in Ji Le Pian by Zhuang Jisu (Southern Song Dynasty), in the Book of Tree Planting by Yu Zhen Mu (Ming Dynasty), in the book Guangdong Xing Yu (17th century), Lingnan by Wu Zhen Fang (Qing Dynasty), in Nanyue Miscellanies by Li Diao Yuan, and others.[6]

Biological control techniques as we know them today started to emerge in the 1870s. During this decade, in the US, the Missouri State Entomologist C. V. Riley and the Illinois State Entomologist W. LeBaron began within-state redistribution of parasitoids to control crop pests. The first international shipment of an insect as biological control agent was made by Charles V. Riley in 1873, shipping to France the predatory mites Tyroglyphus phylloxera to help fight the grapevine phylloxera (Daktulosphaira vitifoliae) that was destroying grapevines in France. The United States Department of Agriculture (USDA) initiated research in classical biological control following the establishment of the Division of Entomology in 1881, with C. V. Riley as Chief. The first importation of a parasitoidal wasp into the United States was that of the braconid Cotesia glomerata in 1883–1884, imported from Europe to control the invasive cabbage white butterfly, Pieris rapae. In 1888–1889 the vedalia beetle, Rodolia cardinalis, a lady beetle, was introduced from Australia to California to control the cottony cushion scale, Icerya purchasi. This had become a major problem for the newly developed citrus industry in California, but by the end of 1889 the cottony cushion scale population had already declined. This great success led to further introductions of beneficial insects into the USA.[7][8]

In 1905 the USDA initiated its first large-scale biological control program, sending entomologists to Europe and Japan to look for natural enemies of the gypsy moth, Lymantria dispar dispar, and brown-tail moth, Euproctis chrysorrhoea, invasive pests of trees and shrubs. As a result, nine parasitoids (solitary wasps) of gypsy moth, seven of brown-tail moth, and two predators of both moths became established in the USA. Although the gypsy moth was not fully controlled by these natural enemies, the frequency, duration, and severity of its outbreaks were reduced and the program was regarded as successful. This program also led to the development of many concepts, principles, and procedures for the implementation of biological control programs.[7][8][9]

Prickly pear cacti were introduced into Queensland, Australia as ornamental plants, starting in 1788. They quickly spread to cover over 25 million hectares of Australia by 1920, increasing by 1 million hectares per year. Digging, burning and crushing all proved ineffective. Two control agents were introduced to help control the spread of the plant, the cactus moth Cactoblastis cactorum, and the scale insect Dactylopius. Between 1926 and 1931, tens of millions of cactus moth eggs were distributed around Queensland with great success, and by 1932, most areas of prickly pear had been destroyed.[10]

The first reported case of a classical biological control attempt in Canada involves the parasitoidal wasp Trichogramma minutum. Individuals were caught in New York State and released in Ontario gardens in 1882 by William Saunders, trained chemist and first Director of the Dominion Experimental Farms, for controlling the invasive currantworm Nematus ribesii. Between 1884 and 1908, the first Dominion Entomologist, James Fletcher, continued introductions of other parasitoids and pathogens for the control of pests in Canada.[11]

Types of biological pest control[]

There are three basic biological pest control strategies: importation (classical biological control), augmentation and conservation.[12]

Importation[]

Importation or classical biological control involves the introduction of a pest's natural enemies to a new locale where they do not occur naturally. Early instances were often unofficial and not based on research, and some introduced species became serious pests themselves.[13]

To be most effective at controlling a pest, a biological control agent requires a colonizing ability which allows it to keep pace with changes to the habitat in space and time. Control is greatest if the agent has temporal persistence, so that it can maintain its population even in the temporary absence of the target species, and if it is an opportunistic forager, enabling it to rapidly exploit a pest population.[14]

Joseph Needham noted a Chinese text dating from 304 AD, Records of the Plants and Trees of the Southern Regions, by Hsi Han, which describes mandarin oranges protected by large reddish-yellow citrus ants which attack and kill insect pests of the orange trees. The citrus ant (Oecophylla smaragdina)[15] was rediscovered in the 20th century, and since 1958 has been used in China to protect orange groves.[16]

Damage from Hypera postica, the alfalfa weevil, a serious introduced pest of forage, was substantially reduced by the introduction of natural enemies. 20 years after their introduction the population of weevils in the alfalfa area treated for alfalfa weevil in the Northeastern United States remained 75 percent down.[19]

Augmentation[]

Augmentation involves the supplemental release of natural enemies that occur in a particular area, boosting the naturally occurring populations there. In inoculative release, small numbers of the control agents are released at intervals to allow them to reproduce, in the hope of setting up longer-term control, and thus keeping the pest down to a low level, constituting prevention rather than cure. In inundative release, in contrast, large numbers are released in the hope of rapidly reducing a damaging pest population, correcting a problem that has already arisen. Augmentation can be effective, but is not guaranteed to work, and depends on the precise details of the interactions between each pest and control agent.[26]

The egg parasite Trichogramma is frequently released inundatively to control harmful moths. Similarly, Bacillus thuringiensis and other microbial insecticides are used in large enough quantities for a rapid effect.[26] Recommended release rates for Trichogramma in vegetable or field crops range from 5,000 to 200,000 per acre (1 to 50 per square metre) per week according to the level of pest infestation.[29] Similarly, nematodes that kill insects (that are entomopathogenic) are released at rates of millions and even billions per acre for control of certain soil-dwelling insect pests.[30]

Conservation[]

The conservation of existing natural enemies in an environment is the third method of biological pest control.[31]
Natural enemies are already adapted to the habitat and to the target pest, and their conservation can be simple and cost-effective, as when nectar-producing crop plants are grown in the borders of rice fields. These provide nectar to support parasitoids and predators of planthopper pests and have been demonstrated to be so effective (reducing pest densities by 10- or even 100-fold) that farmers sprayed 70% less insecticides and enjoyed yields boosted by 5%.[32] Predators of aphids were similarly found to be present in tussock grasses by field boundary hedges in England, but they spread too slowly to reach the centres of fields. Control was improved by planting a metre-wide strip of tussock grasses in field centres, enabling aphid predators to overwinter there.[31]

Cropping systems can be modified to favor natural enemies, a practice sometimes referred to as habitat manipulation. Providing a suitable habitat, such as a shelterbelt, hedgerow, or beetle bank where beneficial insects such as parasitoidal wasps can live and reproduce, can help ensure the survival of populations of natural enemies. Things as simple as leaving a layer of fallen leaves or mulch in place provides a suitable food source for worms and provides a shelter for insects, in turn being a food source for such beneficial mammals as hedgehogs and shrews. Compost piles and stacks of wood can provide shelter for invertebrates and small mammals. Long grass and ponds support amphibians. Not removing dead annuals and non-hardy plants in the autumn allows insects to make use of their hollow stems during winter.[33] In California, prune trees are sometimes planted in grape vineyards to provide an improved overwintering habitat or refuge for a key grape pest parasitoid.[34] The providing of artificial shelters in the form of wooden caskets, boxes or flowerpots is also sometimes undertaken, particularly in gardens, to make a cropped area more attractive to natural enemies. For example, earwigs are natural predators which can be encouraged in gardens by hanging upside-down flowerpots filled with straw or wood wool. Green lacewings can be encouraged by using plastic bottles with an open bottom and a roll of cardboard inside. Birdhouses enable insectivorous birds to nest; the most useful birds can be attracted by choosing an opening just large enough for the desired species.[33]

In cotton production, the replacement of broad-spectrum insecticides with selective control measures such as Bt cotton can create a more favorable environment for natural enemies of cotton pests due to reduced insecticide exposure risk. Such predators or parasitoids can control pests not affected by the Bt protein. Reduced prey quality and abundance associated increased control from Bt cotton can also indirectly decrease natural enemy populations in some cases, but the percentage of pests eaten or parasitized in Bt and non-Bt cotton are often similar.[35]

Biological control agents[]

Predators[]

Predators are mainly free-living species that directly consume a large number of prey during their whole lifetime. Given that many major crop pests are insects, many of the predators used in biological control are insectivorous species. Lady beetles, and in particular their larvae which are active between May and July in the northern hemisphere, are voracious predators of aphids, and also consume mites, scale insects and small caterpillars. The spotted lady beetle (Coleomegilla maculata) is also able to feed on the eggs and larvae of the Colorado potato beetle (Leptinotarsa decemlineata).[36]

The larvae of many hoverfly species principally feed upon aphids, one larva devouring up to 400 in its lifetime. Their effectiveness in commercial crops has not been studied.[37]

Several species of entomopathogenic nematode are important predators of insect and other invertebrate pests.[38]Phasmarhabditis hermaphrodita is a microscopic nematode that kills slugs. Its complex life cycle includes a free-living, infective stage in the soil where it becomes associated with a pathogenic bacteria such as Moraxella osloensis. The nematode enters the slug through the posterior mantle region, thereafter feeding and reproducing inside, but it is the bacteria that kill the slug. The nematode is available commercially in Europe and is applied by watering onto moist soil.[39]

Predators including Cactoblastis cactorum (mentioned above) can also be used to destroy invasive plant species. As another example, the poison hemlock moth (Agonopterix alstroemeriana) can be used to control poison hemlock (Conium maculatum). During its larval stage, the moth strictly consumes its host plant, poison hemlock, and can exist at hundreds of larvae per individual host plant, destroying large swathes of the hemlock.[43]

For rodent pests, cats are effective biological control when used in conjunction with reduction of "harborage"/hiding locations.[45][46][47] While cats are effective at preventing rodent "population explosions", they are not effective for eliminating pre-existing severe infestations.[47]Barn owls are also sometimes used as biological rodent control.[48] Although there are no quantitative studies of the effectiveness of barn owls for this purpose,[49] they are known rodent predators that can be used in addition to or instead of cats;[50][51] they can be encouraged into an area with nest boxes.[52][53]

Parasitoids[]

Parasitoids lay their eggs on or in the body of an insect host, which is then used as a food for developing larvae. The host is ultimately killed. Most insect parasitoids are wasps or flies, and many have a very narrow host range. The most important groups are the ichneumonid wasps, which mainly use caterpillars as hosts; braconid wasps, which attack caterpillars and a wide range of other insects including aphids; chalcid wasps, which parasitize eggs and larvae of many insect species; and tachinid flies, which parasitize a wide range of insects including caterpillars, beetle adults and larvae, and true bugs.[54] Parasitoids are most effective at reducing pest populations when their host organisms have limited refuges to hide from them.[55]

Parasitoids are among the most widely used biological control agents. Commercially, there are two types of rearing systems: short-term daily output with high production of parasitoids per day, and long-term, low daily output systems.[56] In most instances, production will need to be matched with the appropriate release dates when susceptible host species at a suitable phase of development will be available.[57] Larger production facilities produce on a yearlong basis, whereas some facilities produce only seasonally. Rearing facilities are usually a significant distance from where the agents are to be used in the field, and transporting the parasitoids from the point of production to the point of use can pose problems.[58] Shipping conditions can be too hot, and even vibrations from planes or trucks can adversely affect parasitoids.[56]

The eastern spruce budworm is an example of a destructive insect in fir and spruce forests. Birds are a natural form of biological control, but the Trichogramma minutum, a species of parasitic wasp, has been investigated as an alternative to more controversial chemical controls.[60]

Pathogens[]

Pathogenic micro-organisms include bacteria, fungi, and viruses. They kill or debilitate their host and are relatively host-specific. Various microbial insect diseases occur naturally, but may also be used as biological pesticides.[61] When naturally occurring, these outbreaks are density-dependent in that they generally only occur as insect populations become denser.[62]

Bacteria[]

Bacteria used for biological control infect insects via their digestive tracts, so they offer only limited options for controlling insects with sucking mouth parts such as aphids and scale insects.[63]Bacillus thuringiensis, a soil-dwelling bacterium, is the most widely applied species of bacteria used for biological control, with at least four sub-species used against Lepidopteran (moth, butterfly), Coleopteran (beetle) and Dipteran (true fly) insect pests. The bacterium is available to organic farmers in sachets of dried spores which are mixed with water and sprayed onto vulnerable plants such as brassicas and fruit trees.[64][65]Genes from B. thuringiensis have also been incorporated into transgenic crops, making the plants express some of the bacterium's toxins, which are proteins. These confer resistance to insect pests and thus reduce the necessity for pesticide use.[66] If pests develop resistance to the toxins in these crops, B. thuringiensis will become useless in organic farming also.[67][65]
The bacterium Paenibacillus popilliae which causes milky spore disease has been found useful in the control of Japanese beetle, killing the larvae. It is very specific to its host species and is harmless to vertebrates and other invertebrates.[68]

Viruses[]

Baculoviruses are specific to individual insect host species and have been shown to be useful in biological pest control. For example, the Lymantria dispar multicapsid nuclear polyhedrosis virus has been used to spray large areas of forest in North America where larvae of the gypsy moth are causing serious defoliation. The moth larvae are killed by the virus they have eaten and die, the disintegrating cadavers leaving virus particles on the foliage to infect other larvae.[77]

A mammalian virus, the rabbit haemorrhagic disease virus was introduced to Australia to attempt to control the European rabbit populations there.[78] It escaped from quarantine and spread across the country, killing large numbers of rabbits. Very young animals survived, passing immunity to their offspring in due course and eventually producing a virus-resistant population.[79] Introduction into New Zealand in the 1990s was similarly successful at first, but a decade later, immunity had developed and populations had returned to pre-RHD levels.[80]

Oomycota[]

Lagenidium giganteum is a water-borne mould that parasitizes the larval stage of mosquitoes. When applied to water, the motile spores avoid unsuitable host species and search out suitable mosquito larval hosts. This mould has the advantages of a dormant phase, resistant to desiccation, with slow-release characteristics over several years. Unfortunately, it is susceptible to many chemicals used in mosquito abatement programmes.[81]

Combined use of parasitoids and pathogens[]

In cases of massive and severe infection of invasive pests, techniques of pest control are often used in combination. An example is the emerald ash borer, Agrilus planipennis, an invasive beetle from China, which has destroyed tens of millions of ash trees in its introduced range in North America. As part of the campaign against it, from 2003 American scientists and the Chinese Academy of Forestry searched for its natural enemies in the wild, leading to the discovery of several parasitoid wasps, namely Tetrastichus planipennisi, a gregarious larval endoparasitoid, Oobius agrili, a solitary, parthenogenic egg parasitoid, and Spathius agrili, a gregarious larval ectoparasitoid. These have been introduced and released into the United States of America as a possible biological control of the emerald ash borer. Initial results for Tetrastichus planipennisi have shown promise, and it is now being released along with Beauveria bassiana, a fungal pathogen with known insecticidal properties.[85][86][87]

Difficulties[]

Many of the most important pests are exotic, invasive species that severely impact agriculture, horticulture, forestry and urban environments. They tend to arrive without their co-evolved
parasites, pathogens and predators, and by escaping from these, populations may soar. Importing the natural enemies of these pests may seem a logical move but this may have unintended consequences; regulations may be ineffective and there may be unanticipated effects on biodiversity, and the adoption of the techniques may prove challenging because of a lack of knowledge among farmers and growers.[88]

Side effects[]

Biological control can affect biodiversity[14] through predation, parasitism, pathogenicity, competition, or other attacks on non-target species.[89] An introduced control does not always target only the intended pest species; it can also target native species.[90] In Hawaii during the 1940s parasitic wasps were introduced to control a lepidopteran pest and the wasps are still found there today. This may have a negative impact on the native ecosystem; however, host range and impacts need to be studied before declaring their impact on the environment.[91]

Cane toad (introduced into Australia 1935) spread from 1940 to 1980: it was ineffective as a control agent. Its distribution has continued to widen since 1980.

Vertebrate animals tend to be generalist feeders, and seldom make good biological control agents; many of the classic cases of "biocontrol gone awry" involve vertebrates. For example, the cane toad (Rhinella marina) was intentionally introduced to Australia to control the greyback cane beetle (Dermolepida albohirtum),[92] and other pests of sugar cane. 102 toads were obtained from Hawaii and bred in captivity to increase their numbers until they were released into the sugar cane fields of the tropic north in 1935. It was later discovered that the toads could not jump very high and so were unable to eat the cane beetles which stayed on the upper stalks of the cane plants. However, the toad thrived by feeding on other insects and soon spread very rapidly; it took over native amphibianhabitat and brought foreign disease to native toads and frogs, dramatically reducing their populations. Also, when it is threatened or handled, the cane toad releases poison from parotoid glands on its shoulders; native Australian species such as goannas, tiger snakes, dingos and northern quolls that attempted to eat the toad were harmed or killed. However, there has been some recent evidence that native predators are adapting, both physiologically and through changing their behaviour, so in the long run, their populations may recover.[93]

Rhinocyllus conicus, a seed-feeding weevil, was introduced to North America to control exotic musk thistle (Carduus nutans) and Canadian thistle (Cirsium arvense). However, the weevil also attacks native thistles, harming such species as the endemicPlatte thistle (Cirsium neomexicanum) by selecting larger plants (which reduced the gene pool), reducing seed production and ultimately threatening the species' survival.[94]

The small Asian mongoose (Herpestus javanicus) was introduced to Hawaii in order to control the rat population. However, the mongoose was diurnal, and the rats emerged at night; the mongoose therefore preyed on the endemic birds of Hawaii, especially their eggs, more often than it ate the rats, and now both rats and mongooses threaten the birds. This introduction was undertaken without understanding the consequences of such an action. No regulations existed at the time, and more careful evaluation should prevent such releases now.[95]

The sturdy and prolific eastern mosquitofish (Gambusia holbrooki) is a native of the southeastern United States and was introduced around the world in the 1930s and '40s to feed on mosquito larvae and thus combat malaria. However, it has thrived at the expense of local species, causing a decline of endemic fish and frogs through competition for food resources, as well as through eating their eggs and larvae.[96] In Australia, control of the mosquitofish is the subject of discussion; in 1989 researchers A. H. Arthington and L. L. Lloyd stated that "biological population control is well beyond present capabilities".[97]

Grower education[]

A potential obstacle to the adoption of biological pest control measures is that growers may prefer to stay with the familiar use of pesticides. However, pesticides have undesired effects, including the development of resistance among pests, and the destruction of natural enemies; these may in turn enable outbreaks of pests of other species than the ones originally targeted, and on crops at a distance from those treated with pesticides.[98] One method of increasing grower adoption of biocontrol methods involves letting them learn by doing, for example showing them simple field experiments, enabling them to observe the live predation of pests, or demonstrations of parasitised pests. In the Philippines, early season sprays against leaf folder caterpillars were common practice, but growers were asked to follow a 'rule of thumb' of not spraying against leaf folders for the first 30 days after transplanting; participation in this resulted in a reduction of insecticide use by 1/3 and a change in grower perception of insecticide use.[99]

^ abCoulson, J. R.; Vail, P. V.; Dix M.E.; Nordlund, D.A.; Kauffman, W.C.; Eds. 2000. 110 years of biological control research and development in the United States Department of Agriculture: 1883–1993. U.S. Department of Agriculture, Agricultural Research Service. pages=3–11

^Capinera, John L. (October 2005). "Featured creatures: Peach Aphid". University of Florida – Department of Entomology and Nematology. University of Florida. Archived from the original on 26 May 2016. Retrieved 7 June 2016.